Malformed frogs: The collapse of aquatic ecosystems

Malformed Frogs: The Collapse of Aquatic Ecosystems

Volumn , Issue , 2008, Pages

  Lannoo, Michael ^a  

^a INDIANA UNIVERSITY SCHOOL OF MEDICINE   (United States)

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References (510)

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12. At the Indiana University School of Medicine, where I teach, we have adopted a competency-based curriculum, that centers on the following: effective communication; basic clinical skills; using science to guide diagnosis, management, therapeutics, and prevention; lifelong learning; self-awareness, self-care, and personal growth; social and community contexts of health care; moral reasoning and ethical judgment; problem solving; and professionalism and role recognition.
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23. Much of the information I present here on vertebrate development is well known and well represented in texts on embryology. In assembling this chapter I have relied on a variety of sources that were important to my initial learning of this material, including:
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29. Johnson, P.T.J., K.B. Lunde, R.W. Haight, J. Bowerman and A.R. Blaustein. 2001. Ribeiroia ondatrae (Trematoda: Digena) infection induces severe limb malformations in western toads (Bufo boreas). Canadian Journal of Zoology 79:370-379-
30. Johnson, P.T.J., K.B. Lunde, E.G. Ritchie, J.K. Reaser and A.E. Launer. 2001. Morphological abnormality patterns in a California amphibian community. Herpetologica 57:336-352.
31. Johnson, P.T.J., K.B. Lunde, E.M. Thurman, E.G. Ritchie, S.N. Wray, D.R. Sutherland, J.M. Kapfer, T.J. Frest, J. Bowerman and A.R. Blaustein. 2002. Parasite (Ribeiroia ondatrae) infection linked to amphibian malformations in the western United States. Ecological Monographs 72:151-168.
32. Johnson, P.T.J, and K.B. Lunde. 2005. Parasite infection and limb malformations: A growing problem in amphibian conservation, pp. 124-138 in Lannoo, M.J. (Ed.), Amphibian Declines: The Conservation Status of United States Species. University of California Press, Berkeley, California.
33. Johnson, P.T.J., J.M. Chase, K. L. Dosch, R.B. Hartson, J.A. Gross, D.J. Larson, D.R. Sutherland and S.R. Carpenter. 2007. Aquatic eutrophication promotes pathogenic infection in amphibians. Proceedings of the National Academy of Science 104:15781-15786.
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37. Lannoo, M.J., D.R. Sutherland, P. Jones, D. Rosenberry, R.W. Klaver, D.M. Hoppe, P.T.J. Johnson, K.B. Lunde, C. Facemire and J.M. Kapfer. 2003. Multiple causes for the malformed frog phenomenon, pp. 233-262 in Linder, G., S. Krest, D. Sparling and E. Little (Eds.), Multiple Stressor Effects in Relation to Declining Amphibian Populations. American Society for Testing Materials International, West Conshoshocken, Pennsylvania.
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61. Gardiner, D.M. and D.M. Hoppe. 1999. Environmentally induced limb mal formations in mink frogs (Rana septentrionalis). Journal of Experimental Zoology 284:207-216.
62. Takeishi, M. 1996. On the frog, Rana ornativentralis, with supernumerary limbs found at Yamada Greenery area in Kitakyushu City, Fukuoka Prefecture. Japan Bulletin of the Kitakyushu Museum of Natural History 15:119-131.
63. Summarized in: Gardiner, D.M. and D.M. Hoppe. 1999. Environmentally induced limb malformations in mink frogs {Rana septentrionalis). Journal of Experimental Zoology 284:207-216.
64. See also: Burke, A.C. and C. Tabin. 1996. Virally mediated misexpression of Hoxc-6 in the cervical mesoderm results in spinal nerve truncations. Developmental Biology 178:192-197.
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68. Gibson-Brown, J.J., S.I. Agulnik, L.M. Silver, L. Niswander and V.E. Papaioannou. 1996. Involvement of T-box genes Tbx2-Tbx5 in vertebrate limb specification and development. Development 125:2499-2509.
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73. Ankley, G.T., J.E. Tietge, D.L. DeFoe, K.M.Jensen, G.W. Holcombe, E.J. Durhan and S.A. Diamond. 1998. Effects of ultraviolet light and methoprene on survival and development of Rana pipiens. Environmental Toxicology and Chemistry 17:2530-2542.
74. Ankley, G.T., J.E. Tietge, G.W. Holcombe, D.L. DeFoe, S.A. Diamond, K.M.Jensen and S.J. Degitz. 2000. Effects of laboratory ultraviolet radiation and natural sunlight on survival and development of Rana pipiens. Canadian Journal of Zoology 78:1092-1100.
75. Ankley, G.T., S.A. Diamond, J.E. Tietge, G.W. Holcombe, K.M.Jensen, D.L. DeFoe and R. Peterson. 2002. Assessment of the risk of solar ultraviolet radiation to amphibians. I. Dose dependent induction of hindlimb malformations in the northern leopard frog (Rana pipiens). Environmental Science and Technology 36:2853-2858.
76. See also: Bilski, P., J.G. Burkhart and C.F. Chignell. 2003. Photochemical characterization of water samples from Minnesota and Vermont sites with malformed frogs: potential influence of photosensitization by singlet molecular oxygen and free radicals on aquatic toxicology. Aquatic Toxicology 65:229-241.
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79. Stopper, G.F., L. Hecker, R.A. Franssen and S.S. Sessions. 2002. How trema-todes cause limb deformities in amphibians. Journal of Experimental Zoology Part B: Molecular and Developmental Evolution 294:252-263.
80. Johnson, P.T.J., K.B. Lunde, D.A. Zelmer andJ.K. Werner. 2003. Limb deformities as an emerging parasitic disease in amphibians. Conservation Biology 17:1724-1737 (p. 1728).
81. Johnson, P.T.J., K.B. Lunde, E.G. Ritchie and A.E. Launer. 1999. The effect of trematode infection on amphibian limb development and survivorship. Science 284:802-804.
82. See also: Johnson, P.T.J., J.M. Chase, K. L. Dosch, R.B. Hartson, J.A. Gross, D.J. Larson, D.R. Sutherland and S.R. Carpenter. 2007. Aquatic eutrophication promotes pathogenic infection in amphibians. Proceedings of the National Academy of Science 104:15781-15786.
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84. Johnson, P.T.J., K.B. Lunde, D.A. Zelmer andJ.K. Werner. 2003. Limb deformities as an emerging parasitic disease in amphibians. Conservation Biology 17:1724-1737.
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88. Ecoregions indicated are U.S. E.P.A. Level III ecoregions as defined by the following article: United States Environmental Protection Agency (USEPA). 2000. Level III ecoregions of the continental United States (revision of Omernik, 1987, see below), Map M-i. USEPA National Health and Environmental Effects Research Laboratory, Corvallis, Oregon.
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93. See also: Ouellet, M., J. Bonin, J. Rodrigue, J.-L. DesGranges and S. Lair. 1997. Hindlimb deformities (ectromelia, ectrodactyly) in free-living anurans from agricultural habitats. Journal of Wildlife Diseases 33:95-104.
94. Johnson, P.T.J., K.B. Lunde, E.G. Ritchie, J.K. Reaser and A.E. Launer. 2001. Morphological abnormality patterns in a California amphibian commu nity. Herpetologica 57:336-352.
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106. See also: Ovaska, K., T.M. Davis and I.N. Flamarique. 1997. Hatching success and larval survival of the frogs Hyla regilla and Rana aurora under ambient and artificially enhanced solar ultraviolet radiation. Canadian Journal of Zoology 75:1081-1088.
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108. Tietge, J.E., S.A. Diamond, G.T. Ankley, D.L. DeFoe, G.W. Holcombe, K.M. Jensen, S.J. Degitz, G.E. Elonen and E. Hammer. 2001. Ambient solar UV radiation causes mortality in larvae of three species of Rana under controlled exposure conditions. Photochemistry and Photobiology 74:261-268.
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111. Ankley, G.T., J.E. Tietge, G.W. Holcombe, D.L. DeFoe, S.A. Diamond, K.M. Jensen and S.J. Degitz. 2000. Effects of laboratory ultraviolet radiation and natural sunlight on survival and development of Rana pipiens. Canadian Journal of Zoology 78:1092-1100.
112. Ankley, G.T., S.A. Diamond, J.E. Tietge, G.W. Holcombe, K.M. Jensen, D.L. DeFoe and R. Peterson. 2002. Assessment of the risk of solar ultraviolet radiation to amphibians. I. Dose-dependent induction of hindlimb malformations in the northern leopard frog (Rana pipiens). Environmental Science and Technology 36:2853-2858.
113. See also: Skelly, D.K., S.R. Bolden, M.P. Holland, L.K. Freidenburg, N.A. Freidenfelds and T.R. Malcolm. 2006. Urbanization and disease in amphibians. Pp. 153-167. In Collinge, S. and C. Ray (Eds.), Ecology of Disease: Community Context and Pathogen Dynamics. Oxford University Press, Oxford, England.
114. Also: Forson, D.D. and A. Storfer. 2006. Atrazine increases ranavirus susceptibility in the tiger salamander, Ambystoma tigrinum. Ecological Applications 16:2325-2332.
115. Johnson, P.T.J., K.B. Lunde, E.G. Ritchie and A.E. Launer. 1999. The effect of trematode infection on amphibian limb development and survivorship. Science 284:802-804.
116. Johnson, P.T.J., K.B. Lunde, R.W. Haight, J. Bowerman and A.R. Blaustein. 2001. Ribeiroia ondatrae (Trematoda: Digena) infection induces severe limb malformations in western toads (Bufo boreas). Canadian Journal of Zoology 79:370-379.
117. Johnson, P.T.J., K.B. Lunde, E.G. Ritchie, J.K. Reaser and A.E. Launer. 2001. Morphological abnormality patterns in a California amphibian community. Herpetologica 57:336-352.
118. Johnson, P.T.J., K.B. Lunde, E.M. Thurman, E.G. Ritchie, S.N. Wray, D.R. Sutherland, J.M. Kapfer, T.J. Frest, J. Bowerman and A.R. Blaustein. 2002. Parasite (Ribeiroia ondatrae) infection linked to amphibian malformations in the western United States. Ecological Monographs 72:151-168.
119. Johnson, P.T.J. and K.B. Lunde. 2005. Parasite infection and limb malformations: a growing problem in amphibian conservation. Pp. 124-138. In Lannoo, M.J. (Ed.), Amphibian Declines: The Conservation Status of United States Species. University of California Press, Berkeley, California.
120. See also: Johnson, P.T.J., J.M. Chase, K. L. Dosch, R.B. Hartson, J.A. Gross, D.J. Larson, D.R. Sutherland and S.R. Carpenter. 2007. Aquatic eutrophication promotes pathogenic infection in amphibians. Proceedings of the National Academy of Science 104:15781-15786.
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122. Forson, D.D. and A. Storfer. 2006. Atrazine increases ranavirus susceptibility in the tiger salamander, Ambystoma tigrinum. Ecological Applications 16:2325-2332.
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127. Reylea, R.A. and N. Mills. 2001. Predator-induced stress makes the pesticide carbaryl more deadly to gray treefrog tadpoles (Hyla versicolor). Proceedings of the National Academy of Sciences 98:2491-2496.
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